Ringelstein Et Al
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J. Mar. Biol. Ass. U.K. (2006), 86, 909^918 Printed in the United Kingdom
Food and feeding ecology of the striped dolphin, Stenella coeruleoalba, in the oceanic waters of the north-east Atlantic Julien Ringelstein*, Claire Pusineri*, Sami HassaniO, Laureline Meynier*P, Re¤mi Nicolas* and Vincent Ridoux*P$ *Centre de Recherche sur les Ecosyste'mes Littoraux Anthropise¤s, UMR6217, Universite¤ de La Rochelle, 17071 La Rochelle cedex, France. OLaboratoire d0 Etude des Mammife'res Marins, Oce¤anopolis, BP411, 29275 Brest cedex, France. P Centre de Recherche sur les Mammife'res Marins, Universite¤ de La Rochelle, 17071 La Rochelle, France. $ Corresponding author, e-mail: [email protected]
The food and feeding ecology of the striped dolphin, Stenella coeruleoalba, in the oceanic waters of the north-east Atlantic were studied using the stomach contents of 60 striped dolphins caught in the albacore drift-net ¢shery throughout the summer months of 1992 and 1993 o¡ the Bay of Biscay. Thirty-eight per cent of these dolphins were calves (0^1 years old), 25% were juveniles (2^8) and 37% were mature adults (9^32, of which 7 females and 14 males). The diet was found to be primarily composed of ¢sh (39% by mass (M)) and cephalopods (56% M) and secondarily of crustaceans (5% M). The most signi¢cant ¢sh family identi¢ed was the lantern¢sh (24% M) with Notoscopelus kroeyeri and Lobianchia gemellarii being predominant. Among squid, the oceanic Teuthowenia megalops and Histioteuthis spp. were the most signi¢cant. The pelagic shrimp Sergastes arcticus and Pasiphaea multidentata were the most prevalent crustaceans. Prey sizes ranging from 30 to 170 mm accounted for 80% of the prey items while 80% of the reconstituted biomass consisted of prey measuring between 60 and 270 mm. Prey composition and size-range di¡ered slightly with sex and age or body size of the dolphins. The state of digestion of food remains suggested that predation took place at dusk or during the early hours of the night on which the dolphins were caught.
INTRODUCTION The striped dolphin (Stenella coeruleoalba, Meyen, 1833) is a small cetacean distributed worldwide in tropical and warm-temperate waters (Archer, 2002). In the North Atlantic, the species ranges to the west from Newfoundland to the Caribbean with eastern limits from Norway to the Gulf of Guinea (Archer & Perrin, 1999). The species has been reported at water temperatures of 10 to 268C, although most records show temperatures varying from 18 to 228C (Archer & Perrin, 1999). The habitat of the striped dolphin is mainly oceanic, with few incursions over the continental shelf being recorded throughout the range of the species (Archer, 2002). In the water column, the striped dolphin is purported to dive as deep as 200^700 m; however, investigation of its diving and foraging behaviour is not extensive (Archer, 2002). In the north-east Atlantic, the striped dolphin is part of a pelagic top predator community. This is composed mainly of two delphinids, the common Delphinus delphis and the striped dolphin S. coeruleoalba, the blue shark Prionace glauca, the albacore tuna Thunnus alalunga, the sword¢sh Xiphias gladius, and several smaller ¢sh predators including juvenile wreck¢sh Polyprion americanus and the Atlantic pomfret Brama brama. The status of each of these species with regards to ¢sheries is very di¡erent. The albacore tuna and the sword¢sh are target species of directed ¢sheries, the blue shark, the wreck¢sh and the Atlantic pomfret are secondary catches in the Journal of the Marine Biological Association of the United Kingdom (2006)
tuna ¢shery and are only partially marketed, whereas the two dolphins are protected species. The proper management of such a composite set of species requires understanding the ecology of each species and its relationships within the community, notably in terms of pelagic
Figure 1. Sampling location.
Journal of the Marine Biological Association of the United Kingdom (2006)
14 20
50.1^0.2
50.1^0.2
50.1^50.1
50.1^0.1 2.4^5
0.1
0.1
50.1
50.1 3.5 62.1
6.6
13.1
1.6
6.6 59.0 93.4
9 0
1
4
50.1^0.1
14.8 42.6 1.6 19.7 14.8
50.1
5.1 6.3 8.2 3.5 14.0 0.9 50.1 7.8 0.6 3.0
52.5 52.5 45.9 49.2 75.4 37.7 6.6 54.1 18.0 54.1
16 111
50.1^0.2 0.3^1.2
6.6
0.1 0.8
11.5 26.2
163
0.5^1.2
149
22 190 1 123 42
0.8
49.2
0.7^1.8
100 164
50.1^0.2 0.7^2.2 50.1^50.1 0.3^1.3 0.1^0.7
1.1
44.3
0.3^3.9 0.3^2.7
34
0.1 1.3 50.1 0.7 0.3
1.9 1.2
32.8 21.3
0.1^0.3
73
N
294 365 674 234 718 217 8 465 111 0
0.2
13.1
0.1^0.8
95% CI
1.6^10.4 1.7^13.4 4.2^12.5 0.7^7.9 6.9^21.8 0.5^1.4 50.1^0.1 2^17.8 0.2^1.2 2^4.6
0.4
13.1
%N
137.6 11.9
150.0
112.0 13.3
116.2 54.2
195.1 19
162.8 35.5 138.6 28.1 415.0 180.4 53.6 132.4 39.8
20.8 4.1 61.9 9.2 56.8 17.6 46.5 13.7 52.5 23.8 76.6 16.5 41.8 7.1 52.3 14.4 58.0 10.6
90.0 51.9 77.0 26.6
138.4 46.4
150.7 44.8
31.3 8.1 54.2 13.4
149.5 23.1
79.8 17.6
Mean SD
3.7 4
Mean SD
0.4 0.2 3.9 3.8
70.2^318.3 87.3^288.9
96.5^206.0 45.4^257.9
15.0^65.0 37.4^91.5 5.2^99.8 22.5^143.8 16.5^172.7 51.2^116.7 35.1^54.6 26.8^144.0 36.2^112 5.8 3.1 2.2 1.5 22.0 6.6 6.9 2.5 4.5
0.1 0.2 2.9 1.4 3.9 2.7 1.7 3.7 3.1 7.1 7.4 4.8 2.5 0.4 1.3 2 4.3 0.8 2.7
32.4^157.5 11.5 7.4 10.7^164.5 8.9 4.5
82.4^332.4 13.9 15.3
18.0^303.1 21.4 6.4
5.4^49.5 28.8^97.1
98.0^198.4 38.6 19.7
52.0^157.7
Range
13.6
9.5 1.1
116.9^151.8 45.1 3.9 3.7
97.2^135.0
26.3^206.5 13.0 8.0
38.3^49.8
8.3^11.5
4.5^27.8
6.1^54.8
0.3^35.9 0.5^24.6
0.2 2.4 38.9
50.1
0.2
0.2
0.2
0.1 0.5 0.3 0.8 0.1
0.1 3.2 5.7 1.1 8.2 0.8 50.1 1.9 0.5 1.5
50.1^2.7 0.4^9.8 50.1^17.2 0.1^55.5 0.1^75.8 2.4^27.5 2.1^3.3 0.1^28.2 1.1^6.5 1.2^10.0 0.1^15.9
0.2 1.7
1.9
3.5^20.4 2.1^29.6
0.6^106.4
4.3
0.1 0.8
50.1^1.1 0.4^20.6 2.6^43
1.5
0.2
%M reconstituted
0.1^0.5 1.2^3.8
50.1^50.1
0.1^0.3
50.1^0.4
50.1^0.4
50.1^0.2 0.2^0.8 50.1^0.9 0.3^1.7 50.1^0.3
50.1^0.2 0.7^7.5 2.5^9 0.5^2 4.1^13 0.4^1.5 50.1^50.1 1^3.2 0.2^0.9 0.9^2.5
0.1^0.5 0.2^3.7
1^2.9
2.3^7
50.1^0.3 0.2^1.4
0.5^2.3
50.1^0.3
95% CI
Composition by mass
7.3^98.4
0.8^31.0
Range
Mass (g)
176.5^221.7 23.6 22.1
Length (mm)
6.6 14.8 95.1
13.1
1.6
14.8 42.6 1.6 19.7 14.8
39.3 49.2 44.3 31.1 72.1 36.1 4.9 44.3 18 47.5
9.8 23.0
49.2
6.6
8.2 16.4
11.5
13.1
% Occurrence
0.1 0.7 71.8
0.2
50.1
0.2 2.3 50.1 1.3 0.6
5.1 6.7 14 1.7 20.2 1.4 50.1 7.1 1.1 3.1
0.1 0.8
1.4
0.5
1.3 1.3
0.2
0.6
%N
(Continued)
0.4 0.5 54.6
0.3
50.1
0.2 0.9 0.5 0.9 0.3
0.1 3.4 10.1 1 13.3 1.9 50.1 2 6.5 1.5
0.4 1.8
3.5
2.4
0.1 0.8
1.5
0.5
%M reconstituted
Fresh fraction (N¼8700; M¼47449.8)
J. Ringelstein et al.
Alepocephalidae Xenodermichthys copei Platytroctidae Unid. Platytroctidae Sternoptychidae Maurolicus muelleri Argyropelecus olfersi Chauliodontidae Chauliodus sloani Stomiidae Stomias boa ferox Bathylagidae Bathylagus greyae Unid. Bathylagidae Myctophidae Benthosema glaciale Ceratoscopelus maderensis Lobianchia gemellarii Myctophum puntatum Notoscopelus kroeyeri Symbolophorus veranyi Diaphus metoclampus Lampanyctus spp. Electrona risso Unid. Myctophidae Paralepididae Macroparalepis a⁄nis Arctozenus risso Paralepis atlantica Paralepis coregonoides Unid. Paralepididae Serrivomeridae Serrivomer beani Scomberesocidae Scomberesox saurus Chiasmodontidae Unid. Chiasmodontidae Gempylidae Nesiarchus nasutus Nomeidae Cubiceps gracilis Unidenti¢ed ¢sh Total ¢sh
% Occurrence
Composition by number
Total composition (N¼15129; M¼82124.7)
Table 1. Diet composition of the striped dolphin in the oceanic Bay of Biscay. % N is the percentage by number of the prey, % M the percentage reconstituted biomass. Lengths are standard length for ¢sh, dorsal mantle length for cephalopods and total length without rostrum for crustaceans.
910 Food and feeding ecology of the striped dolphin in north-east Atlantic
Journal of the Marine Biological Association of the United Kingdom (2006)
Unid., unidenti¢ed.
Acanthephyra purpurea Systellapsis debilis Acanthephyra spp. Unidenti¢ed crustaceans Total crustaceans
Acanthephyra pelagica
Pasiphaea silvado Pasiphaea spp. Oplophoridae
Pasiphaea multidentata
Hyperiidae Unid. Hyperiidae Euphausiidae Meganyctyphanes norvegica Unid. Euphausiidae Peneaeidae Funchalia woodwardii Sergestidae Sergestes arcticus Sergia robusta Pasiphaeidae
Octopoteutidae Octopoteuthis sp. Onychoteuthidae Onychoteuthis banksi Ancistroteuthis lichtensteini Gonatidae Gonatus steenstrupi Pholidoteuthidae Pholidoteuthis sp. Histioteuthidae Histioteuthis bonellii Histioteuthis reversa Histioteuthis corona Brachioteuthidae Brachioteuthis riisei Ommastrephidae Unid. Ommastrephidae Chiroteuthidae Chiroteuthis imperator Chiroteuthis sp. Cranchiidae Teuthowenia megalops Sepiolidae Heteroteuthis dispar Unid. Sepiolidae Unidenti¢ed cephalopods Total cephalopods
1.4 50.1 50.1
0.1 0.5 0.1 50.1 0.1 5.3
34.4 1.6 1.6
6.6 14.8 6.6 1.6 6.6 70.5
0.1 0.2 50.1 32.4
8.2 13.1 1.6 96.7
1.7 0.5
10.9
83.6
29.5 23.0
50.1 50.1
6.6 1.6
0.2
50.1
6.6
18.0
50.1^0.1 50.1^50.1
9.9
77.0
0.1 50.1
50.1^0.1
50.1 5.2 1.1
1.6 80.3 36.1
9.8 6.6
50.1^50.1 3.9^7 0.5^2.1
50.1
1.6
0.6
50.1^50.1
3.7
83.6
19.7
50.1^0.1 0.7^1.6
50.1 1.1
6.6 49.2
50.1^0.3 0.2^1 50.1^0.2 50.1^0.1 50.1^0.1
0.7^2.4 50.1^50.1 50.1^0.1
0.5^3.1 0.2^0.9
5 47 12 3 0
123 1 1
128 58
19
10 4
50.1^0.3 50.1^0.1 0.1^0.3
22
10 30
50.1^0.1 50.1^0.2 50.1^50.1
0.2^1.1
1099
5 1
4
869
1 624 115
1
486
5 163
13
8.6^13.7
7^13.5
2.6^5.2
50.1^0.2
0.1
18.0
63.4 2.7 63.8 10.3 43.3 5.7 55.4 4.7
97.9 25.5 114.6 91.9
49.2 5.8 71.7 5.7
109.4 15.1
27.7 3.8 24.2 3.7
16.0 4.3
15.8 0.1 15.9 0.3
106.5 25.5
99.2 9.8 40.7
102.8 68.6
25.7 22.5
265.7 25.7 8.5 23.5 8
124.4
105.6 34
71.3 53.4 57.1 15.8
27.6 49.6
1.9 1.9
501.6 35.4 11.7 42.3 13.9
0.2 0.1 0.1 50.1
0.1 0.1
1.5 0.1 1.6 0.2 19.7
59.1^66.0 5.6^85.2 31.9^51.4 51.2^61.9
6.9^151.8
33.6^72.5 45.2^86.3
2.1 0.3 2.3 1 0.9 0.3 1.4 0.3 6.0
7.3 1.9 11.2 5.7
4.0 4.5 1.6 0.7
94.2^142.5 17.8 9.5
19.8^33.1 18.7^28.1
11.0^23.7
15.7^15.9 15.5^16.6
41.2^200.2 16.4 10.7
81.4^108.5 25.4 6.8 6.7
64.9^243.8 152.3 101.7
15.0^78.0
7.8^56.9 11.6^61.1
144.8
15.8^282.4 43.9 35.6
4.0^128.5 26.1 23.2 31.0^122.7 27.5 44.6
6.4^198.6 81.9 84.9
1.7^2.3 0.1^6.0 0.5^1.4 1.1^1.9
1.9^14.6
3.2^25.3 0.8^3.5
8.2^38.6
0.1^0.3 0.1^0.2
50.1^0.4
1.4^1.6 1.3^2.0
0.9^73.9
13.4^32.5
96.3^361.5
1.1^8.3
10.8^78.9 20.3^106.8
5.0^445.3
0.2^59.5 0.8^326.0
15.4^331.6
50.1 0.2 50.1 50.1 0.1 5.2
1.8 50.1 50.1
2.3 0.2
0.6
50.1 50.1
50.1
50.1 50.1 50.1 55.9
31.9
0.1 50.1
1.1
0.2
0.2 4.6 8.5
0.2
2.4
0.2 5.5
0.9
50.1^0.1 0.1^0.4 50.1^50.1 50.1^50.1 50.1^0.1
0.7^3.2 50.1^50.1 50.1^0.1
0.8^4.6 0.1^0.3
0.3^1.1
50.1^50.1 50.1^50.1
50.1^50.1
50.1^50.1 50.1^50.1 50.1^0.1
25.9^38.5
50.1^0.3 50.1^0.1
0.3^2.3
0.1^0.3
50.1^0.6 3.6^6.1 3.9^14.6
50.1^0.6
1.7^3.4
50.1^0.4 3.2^8.5
0.4^1.8
6.6 14.8 6.6 50.1 0 59
1.6
21.3
24.6 11.5
9.8
9.8 6.6
19.7
8.2 13.1 3.3 96.7
45.9
1.6
1.6
73.8
1.6 70.5 27.9
18.0
6.6 11.5
6.6
50.1 0.8 0.1 50.1 0 6.1
0.1
1.2
1.9 0.4
0.1
0.2 0.1
1
0.1 0.2 0.1 22.1
1.3
50.1
50.1
13.2
50.1 5.9 0.8
0.4
50.1 0.2
0.1
50.1 0.4 50.1 50.1 0 5.4
0.1
1.7
2.6 0.2
0.5
50.1 50.1
50.1
50.1 0.1 0.1 40
4.1
50.1
0.8
8.4
0.4 14.3 6.1
3.5
0.1 1.8
0.5
Food and feeding ecology of the striped dolphin in north-east Atlantic J. Ringelstein et al. 911
912
J. Ringelstein et al.
Food and feeding ecology of the striped dolphin in north-east Atlantic
Figure 2. Prey length-distribution of all species combined. Lengths are standard length for ¢sh, total length for cephalopods and total length without rostrum for crustaceans.
habitat, of resource utilization and partitioning and of its role in the upper food web. In all cases, the quanti¢cation of the diet is paramount to the understanding of these processes. The feeding ecology of the striped dolphin has mainly been investigated in Japan, South Africa, the Mediterranean Sea and the Bay of Biscay (Miyazaki et al., 1973; Desportes, 1985; Wu«rtz & Marale, 1993; Spitz et al., in press). Cephalopods and ¢sh constitute the bulk of the diet and the typical prey pro¢le of the striped dolphin is a pelagic, gregarious, vertically migrating, small sized organism. Data on the food of the striped dolphin in the North Atlantic are limited to stranded individuals and therefore re£ect the species feeding habits in neritic and coastal waters (Desportes, 1985; Spitz et al., in press). Although in many regions stranded cetaceans incorporate a large proportion of by-caught individuals, they are often considered to be biased towards ill or debilitated individuals. In contrast, the present study is based only on bycaught animals which are presumably healthy. Thus, the aim of this work is to provide a quantitative analysis of the diet of the striped dolphin in the oceanic waters of the
north-east Atlantic (longitude 408050 N to 508290 N and latitude 128190 W to 218190 W) and to describe its variability, based on animals caught in the species’ characteristic o¡shore habitat.
MATERIALS AND METHODS Sampling
This work is based on analysis of the stomach contents of 60 striped dolphins caught in an albacore drift-net ¢shery during the summer months (early June to late September) of 1992 and 1993, as part of a study on the impact of this ¢shery on small cetaceans (Goujon, 1996). The study area was located o¡ the Bay of Biscay between longitude 408050 N and 508290 N and latitude 128190 W to 218190 W (Figure 1). The dolphins in question were by-caught at night in commercial drift-nets 2.5 km long with a 20 m vertical spread. They ranged in age from 0+ to 32 y-old and in size from 112 to 226 cm, corresponding to three predominant age-categories: 38% of the individuals were calves (0^2 y-old), 25% were juveniles (2^8), and 37%
Figure 3. Main prey length-distribution. Lengths are standard length for ¢sh and dorsal mantle length for cephalopods. Journal of the Marine Biological Association of the United Kingdom (2006)
Food and feeding ecology of the striped dolphin in north-east Atlantic J. Ringelstein et al. 913 were mature adults (8^32). Among adults, 34% were females and 67% males (Goujon, 1996). The stomachs were dissected onboard and stored frozen at 7208C in polythene bags awaiting further analysis. Sample analysis
Sample analysis was aimed at describing the diet in terms of prey occurrence, relative abundance, reconstituted mass and size-distribution. It was carried out according to a general procedure which is now standard for marine top predators (Pierce & Boyle, 1991; Croxall, 1993). Details are provided in similar works carried out previously in the same area (Spitz et al., in press). Brie£y, the stomach contents were washed through a sieve of 0.2-mm mesh size, the diagnostic parts and fresh prey recovered and identi¢ed to the lowest taxonomic level using published guides (Clarke, 1986; Ha«rko«nen, 1986) and our own reference collection. To minimize overestimation of prey resistant to digestion (e.g. cephalopod beaks: Bigg & Fawcett, 1985), each prey item was scored on a scale speci¢c to the main prey type (¢sh, cephalopods, crustaceans), according to their state of decomposition. This allowed us to determine a ‘fresh fraction’ that would provide a better representation of the composition of the ingested prey than the total stomach content. Diagnostic hard parts such as beaks, otoliths, and carapaces were measured with a digital Vernier calliper ( 0.02 mm), according to accepted standards (Clarke, 1986; Ha«rko«nen, 1986). A random sub-sample of up to 30 diagnostic hard parts per prey species per stomach sample was measured. Individual prey body length and mass were then calculated using relationships either from the literature (Clarke, 1986; Ha«rko«nen, 1986), or ¢t to measurements performed on specimens in our reference collection. For cephalopods, the standard dorsal mantle length (DML) was used in the general description of the diet (Table 1); however, a total body length including arm length was derived from total length to mantle length ratios obtained from published illustrations of the corresponding species (Nesis, 1987) and used in the ¢gure representing overall prey size-distributions as it quali¢es the prey size targeted by the dolphin (Figure 2) better than DML. The occurrence of a given prey taxon was the number of stomachs in which the taxon was observed and its relative abundance was the number of items of the same taxon found in the sample set. The reconstituted biomass of a taxon was the product of the number of individuals in each stomach and its average reconstituted body mass, summed throughout the sample set. Each of these indices was calculated separately for the total content and the fresh fractions. Standard deviations for the compositions by number (% N) and by mass (% M) were generated by bootstrapping (Reynolds & Aebischer, 1991). The bootstrapping routine was written using the R software. Random samples were drawn with replacement, and the procedure was repeated 300 times. An explanatory diagram, the modi¢ed Costello diagram (Amundsen et al., 1996), was built for each predator. This tool is used to characterize diet variability of a predator graphically by plotting prey speci¢c importance for each prey taxa (% Pi, Equation 1) against Journal of the Marine Biological Association of the United Kingdom (2006)
Figure 4. Costello diagram, a scatterplot of all prey species according to their occurrence and their importance by mass.
frequency of occurrence (% Occ, Equation 2) on a twodimensional graph (Figure 4). In the upper left corner of the diagram, each prey species occurs rarely but accounts for a large proportion of the diet when present; hence, if most prey species concentrate here, the predator is characterized by high between-individual variability. In the upper right corner of the diagram, a single prey is present in all individuals and accounts for the total diet. In this case, all predator individuals rely on the same resource. In the lower right corner, prey species occur at high frequency but each only accounts for a small proportion of the food when present. This suggests high within-individual variability in prey preference and low between-individual variability since all individual predators prey upon the same species assemblage. Finally, in the lower left corner of the diagram, individual prey species display both a low occurrence and low relative importance when present. If most prey species concentrate here, the predator shows both within and betweenindividual variability: % Pi ¼ (i Mi /Sti Mti ) 100
(1)
% Occ ¼ (ni /N) 100
(2)
where Mi is the contribution (by mass in this study) of prey taxa i (at species level, in this study) to stomach content, Mti is the total stomach content weight in only those predators with prey i in their stomach; ni is the number of stomachs in which prey taxon i was found and N the total number of stomachs. Discriminant function analyses (DFAs) were performed to look at intra-speci¢c variability of diet composition between gender ^ maturity categories. Discriminant function analysis generates a set of linear combinations (called the discriminant functions) of explanatory variables (here the prey families) that maximizes the discrimination between pre-de¢ned groups (here the gender ^ maturity categories) (Quinn & Keough, 2002). The data used here were the diet composition by mass at prey family level of all individual samples. The maturity
914
J. Ringelstein et al.
Food and feeding ecology of the striped dolphin in north-east Atlantic
Figure 5. Prey/predator length correlation.
categories were determined from the age of the individuals: calves 52 y-old, juveniles 5257 y-old; and adults 57. Age was determined by reading growth layer groups on teeth slides (Goujon, 1996).
RESULTS General description
About 21% of the available stomachs were full and 79% were half full or less. The total mass of examined food material was 17,250 g which represented an average stomach content of 314 g (N¼60; range 1^2,688). Most food material found was highly digested and the total reconstituted mass was 82,125 g, i.e. 4.8 times the mass of food material actually recovered in the stomachs. Diet composition
The diet of the striped dolphin consisted mainly of ¢sh and cephalopods, but also included crustaceans (occurrence: 93.4%, 96.7% and 70.5% respectively). A total of
9410 ¢sh remains was found, belonging to 55 species of 13 families and corresponding to a reconstituted mass of 31,946 g. The remains of 4917 cephalopod individuals were identi¢ed, corresponding to 13 species of 9 families and 45,908 g of reconstituted mass, in addition to 802 crustaceans of 13 species and 6 families, amounting to a reconstructed mass of 4270 g. Hence, the total diet was constituted of 62.1% ¢sh remains by number and 38.9% by mass, but these ¢gures were increased to 71.8% by number and 54.6% by reconstituted mass in the fresh fraction alone. Myctophid were by far the most signi¢cant ¢sh family, representing 49.4% N of all prey items and 23.0% M of the total diet (and as much as 64.8% N and 42.6% M in the fresh fraction). At least nine di¡erent species were found, with Notoscopelus kroeyeri and Lobianchia gemellari being the most important (Table 1). The cephalopods accounted for 32.4% by number and 55.9% by mass of the total diet, but only 22.1% by number and 40.0% by mass of the fresh fraction. They were represented by at least 15 species, of whichTeuthowenia megalops, Brachioteuthi riissei, Histioteuthis reversa and Gonatus steenstrupi were the most signi¢cant. In the total diet, T. megalops ranked ¢rst by mass among all cephalopods, whereas H. reversa and B. riisei ranked ¢rst and second respectively in the fresh fraction (Table 1). Crustaceans made up 5.3% by number and 5.2% by mass of the total diet, and 6.1% by number and 5.4% by mass of the fresh fraction. The sergestid Sergestes arcticus was the most prevalent species followed by the pasiphaeid Pasiphaea multidentata (Table 1). Length-distributions
The striped dolphins under study fed on prey ranging in size from 10 to 540 mm. Within this extended prey sizerange, the distributions by relative abundance and by relative mass showed quite di¡erent pro¢les (Figure 2). Eighty per cent of the prey items measured between 30 and 170 mm with a major mode from 30^100 mm and a very £at secondary mode at 100^200 mm, whereas 80% of the reconstituted mass was accounted for by size-classes from
Figure 6. Intraspeci¢c diet variability through factorial discriminant analysis of gender^maturity groups (&, adult males; &, adult females; *, juveniles; *, calves).
Journal of the Marine Biological Association of the United Kingdom (2006)
Journal of the Marine Biological Association of the United Kingdom (2006)
Brachioteuthidae Sepiolidae Sepiidae Chiroteuthidae Cranchidae Gonatidae Hitioteuthidae Loliginidae Lycoteuthidae Ommastrephidae Onychoteuthidae Other cephalopods Total cephalopods Total crustaceans
Atherinidae Bathylagidae Belonidae Carangidae Chauliodontidae Clupeidae Emmelichthydae Engraulidea Gadidae Gonostomatidae Merluccidae Mugilidae Myctophidae Nemichthydae Paralepididae Sparidae Sternoptychidae Stomiatidae Alepocephalidae Gobiidae Other ¢sh Total ¢sh
%Nb
%Nb
0.9 6.7 9.9 0.4 0.3 0.9 19.3 50.1
0.1 0.1
2.3 80.4
34.3 35.2 37.5
0.9
1.6 27.5
3.4 1.4 0.8 7.28 1.6
1.3 0.4
0.8 91.0
27.4 6.3 0.5 49.8 1
15.3 0.3
49.2
14.2 1.3 3.8
2.9 23.8 11.9
0.4
1.7
15.6
17.6 3.6 0.7
66.3
3.9
1.3
1.3 19.0
1.1
3.1
%M
50.1
2.8 31.2
0.4
0.3
%Nb
Wu«rtz & Marrale, 1993 Mediterranean Sea N¼23 strandings
2.7 9.1
2.2
2.1
Miyazaki et al., 1973 Japan N¼27 incidental catches
Gess, 1984 South Africa N¼15 strandings and incidental catches
6.8 8 50.1
1.6
0.2 0.1 0.4 0.3 2.8
1.0
11.5 92.0
1.0 5.7
66.9
2.1
2.9
8.6
%Nb
28 50.1
7.7
2.3 0.6 5.1 0.3 11.7
0.3
8.4 72.0
1.4 5.1
49.8
6.6
2.9
4.3
%M
Desportes, 1985 French Atlantic coasts N¼34 strandings and incidental catches
Table 2. Diet composition found in the literature. % N is the percentage by number of the prey, % M the percentage reconstituted biomass.
0.8 8.7 0.5
0.6
0.1 1.4 0.1 1.3
50.1 39 50.1
16.2
0.3 17.5 0.2 4.1
0.1 0.5 0.1
50.1 0.7 50.1 61.0 0.1 24.3 1.1 91.2 0.2 3.9 0.3
0.3 50.1
1.7 1.8 0.4
0.2 43.6
12.3
%M
0.5 0.5
0.5 0.1 2.1
0.2 45.2
16.6
%Nb
Spitz et al., in press French Atlantic coast N¼32 strandings
Food and feeding ecology of the striped dolphin in north-east Atlantic J. Ringelstein et al. 915
916
J. Ringelstein et al.
Food and feeding ecology of the striped dolphin in north-east Atlantic
60 to 270 mm, with two modes at about 40^110 mm and 150^250 mm. This latter mode resulted from the larger size-classes, which, although they only made up the tail end of the relative abundance distribution, represented a signi¢cant part of the reconstituted mass. Among the main prey species (Figure 3), the most numerous lantern¢sh N. kroeyeri and L. gemellari contributed to the ¢rst mode of the overall distribution whereas the cephalopod T. megalops, together with other rarer large species of ¢sh and squid, contributed to the second mode. All crustaceans contributed to the ¢rst mode. Costello diagram
Plotting speci¢c importance against occurrence for all prey species (Figure 4) shows that there is not a single pivotal species; instead, an assemblage of mesopelagic ¢sh and squid is targeted by most individual dolphins. Group 1 (G1) is made up of all the species characterized by both a low occurrence and a low speci¢c importance by mass. Group 2 (G2) constitutes the assemblage of common prey species that display intermediate occurrence (25%5Occ560%); it is made up of a combination of mesopelagic species. Finally, Group 3 (G3) is composed of the most recurrent (60%5Occ580%) prey species which included one myctophid and four oceanic squids. Diet variability
Intra-speci¢c diet variability examined across body size-range and between gender ^ maturity categories (calves, juveniles, adult males and adult females) showed weak yet signi¢cant di¡erences. In spite of extensive variations between individuals, the prey size-range increased with dolphin body length (average prey length¼0.03+2.09dolphin length; R2 ¼0.09; P¼0.025; Figure 5). Similarly, diet composition also changed slightly as shown by the DFA performed on stomach composition by mass. The four gender ^ maturity categories segregated fairly well, with the juveniles in the middle of the projection, suggesting that their diet was intermediate between the calf diet and the male and female adult diets (Figure 6, left side). The length of the discriminant function vectors (Figure 6, right side) was generally shorter than 0.5 suggesting that dietary segregation between gender or maturity categories was far from complete. However, it appeared that two crustacean families (Sergestidae and Oplophoridae) together with the gelatinous squid family Cranchiidae are principally part of the calf diet, whereas the longest vectors associated several non-myctophid ¢sh families to the adult female diet. Finally, very few and only short vectors, including the myctophids, headed towards the male part of the scatterplot suggesting that males simply focus their foraging more heavily on this family than the other categories do.
DISCUSSION General assessment of the study
The present work was the ¢rst quantitative analysis of the diet of the striped dolphin in oceanic habitats of the north-east Atlantic. The diet was found to be primarily composed of ¢sh and cephalopods, and secondarily of Journal of the Marine Biological Association of the United Kingdom (2006)
crustaceans. The lantern¢sh was the most important ¢sh family with predominance of Notoscopelus kroeyeri and Lobianchia gemellarii. Among squid, the oceanic Teuthowenia megalops and Histioteuthis spp. were the most signi¢cant. The pelagic shrimps Sergestes arcticus and Pasiphaea multidentata were the most prevalent crustaceans. Prey individuals measuring 30 to 170 mm accounted for 80% of the prey items and sizes from 60 to 70 mm represented 80% of the reconstituted biomass. Prey composition and size-range di¡ered slightly with sex and age or body size of the dolphins. In general, the food remains were in a state of advanced digestion suggesting that predation took place in the early part of the night on which the dolphins were caught. These results were limited by several constraints. In particular, sampling was determined by the spatiotemporal characteristics of the ¢shery within the study area. More individuals were collected from the north-east sector of the area, close to the continental slope, than elsewhere (Figure 1). For the same reason, samples were only collected at the end of the night, from May to September. The analytical procedure was standard and all the limitations associated with stomach content analyses, notably the biases due to di¡erential transit time in the stomach extensively discussed elsewhere (e.g. Bigg & Fawcett, 1985; Jobling & Breiby, 1986), are fully acknowledged here. However, we believe that scoring the state of digestion of the remains of each prey and considering the fresh fraction alone, as proposed here, partly circumvents this di⁄culty. Finally, the sample size of 60 individuals proved to be su⁄cient to describe the diet of the striped dolphin at an acceptable level of certainty as shown by the 95% con¢dence intervals that are provided in Table 1. Comparison with previous research
The food of the striped dolphin has mainly been investigated in Japan, South Africa, the Mediterranean Sea and the neritic part of the Bay of Biscay (quantitative studies: Miyazaki et al., 1973; Desportes, 1985; Wu«rtz & Marale, 1993; Spitz et al., in press). Cephalopods and ¢sh constitute the bulk of the diet at all locations (Table 2), even if crustaceans and annelids were also found. The dominant prey pro¢le arising from these studies is an epi- or mesopelagic, comparatively small-sized, schooling organism. The gut content of animals collected at sea in oceanic habitats (Miyasaki et al., 1973; this study) were entirely composed of oceanic prey taxa, whereas animals found stranded (Desportes, 1985; Spitz et al., in press) show a mixture of oceanic and shelf prey taxa, with the latter often predominating. This suggests that the population segments that were sampled in oceanic habitats do not usually forage over the shelf, even when they are from areas located close to the shelf break, as was the case in the present study. In contrast, materials obtained from stranded dolphins suggest that these animals had been e⁄ciently foraging in both oceanic and shelf habitats. It is unclear if this represents a particular foraging strategy corresponding to a relatively ‘inshore’ sub-unit of striped dolphin populations, or if it is a minor component of a more widely shared foraging repertoire which would be overlooked by at-sea sampling and, on the contrary, overrepresented in stranding data. Lastly, one could consider
Food and feeding ecology of the striped dolphin in north-east Atlantic J. Ringelstein et al. 917 that material obtained from stranded dolphins might be biased because the source of samples would include more sick animals than materials obtained from ¢sheries. Striped dolphin prey size-ranges mostly overlapped in approximately the 3^30 cm range at all localities where this has been documented in detail (Miyasaki et al., 1973; Spitz et al., in press; present work), suggesting that the preferred prey pro¢le remains the same and, hence, that real plasticity in foraging strategy would be limited. However, it is perhaps noteworthy that, at the only neritic locality where this information has been documented, prey smaller than 10 cm provided less than 15% M of the food against *35% M in the present work. Intraspeci¢c variability
Little is known of intraspeci¢c variability in feeding habits. In the north-west Paci¢c, it was shown that immature striped dolphins concentrate on cepahalopods and take a wider diversity of ¢sh whereas adults preferentially eat ¢sh and crustaceans (Miyasaki et al., 1973). In the present work, it appears that the prey composition and size-distribution change slightly with age and gender. This may result from the ontogeny of diving capacity in calves and immatures and from nursing females being limited in their performance by their accompanying calf. Foraging strategy
The striped dolphin foraging depth-range is supposed to be in the 200^700 m strata, but little is known of its actual diving performances, either maximum or routine (Archer, 2002). In this context, all the species found in the present study live within this broad depth-range, and most of them are members of the vertically migrating mesopelagic fauna. Air breathing top predators can exploit this species assemblage either by foraging deeply during daylight, when these organisms are mostly inactive at depths forming the deep scattering layer, or by foraging at night in the surface layer where these organisms migrate nocturnally for their own feeding (Roe et al., 1984). In the absence of any telemetry data documenting a possible nycthemeral pattern in foraging activity, the prey item digestion conditions can shed some light on this issue. Here, most prey remains were highly digested and the stomach content did not contain much fresh material. From digestion time of small prey organisms observed in various predators (Bigg & Fawcett, 1985; Olson & Boggs, 1986), it appears that the dominant digestion condition observed in our samples is reached about 6 h after ingestion; since the samples were all collected during and at the end of the night, this suggests that most of the foraging activity took place at dusk or early night, when deep sea organisms move up to the surface layer. Interestingly, prey items in fresh condition were rare suggesting that the middle of the night might not be as favourable for foraging as dusk and early night are. This may result from prey organisms being less aggregated when they forage than when they migrate up to the surface layer. Niche breadth expressed as species diversity alone would be extremely wide in the present case, but expressed as the diversity of prey pro¢les could be much narrower, since most prey species are ecologically fairly similar. In Journal of the Marine Biological Association of the United Kingdom (2006)
the Costello diagram, the group of anecdotal species (lower left corner) encompasses all the rare species found in the analysis. At intermediate or higher frequency of occurrence, a more limited number of prey species constitutes the core of the diet. Most of these species occur in 40% to 80% of the samples suggesting that all individual striped dolphins forage on the same species assemblage. Hence, the niche breadth would be mainly accounted for by the speci¢c diversity of the mesopelagic fauna rather than by inter-individual variability in striped dolphin feeding strategy.
This work formed part of a large research programme on the role of pelagic top predators in the Bay of Biscay and adjacent Atlantic Ocean. Fundings from Ifremer and CNRS were obtained through the research project ‘Chantier Golfe de Gascogne, Programme National d0 Environnement Co“tier’. The identi¢cation of prey reference specimens was checked by JeanPaul Lagarde're (CREMA, l’Houmeau, France), Jean-Claude Que¤ro (Muse¤um d’Histoire Naturelle, La Rochelle, France), Yves Cherel (CNRS, Chize¤, France), and Begon‹a Santos Vasquez (University of Aberdeen, Aberdeen, UK). We are grateful to Gre¤goire Certain for computing the bootstrap program. All o¡ered their support, their knowledge and their time, and are gratefully acknowledged for their contribution.
REFERENCES Amundsen, P.A., Gabler, H.M. & Staldvik, F.J., 1996. A new approach to graphical analysis of feeding strategy from stomach contents data-modi¢cation of the Costello (1990) method. Journal of Fish Biology, 48, 607^614. Archer, F.I., 2002. Striped dolphin. In Encyclopedia of marine mammals (ed. W.F. Perrin et al.), pp. 1201^1203. New York: Academic Press. Archer, F.I. & Perrin, W.F., 1999. Stenella coeruleoalba. Mammal Spec, 603, 1^9. Bigg, M.A. & Fawcett, I., 1985. Two biases in diet determination of northern fur seals. In Marine mammals and ¢sheries (ed. J.R. Beddington et al.), pp. 277^282. Boston: George Allen and Unwin. Clarke, M.R., 1986. A handbook for the identi¢cation of cephalopod beaks. Oxford: Clarendon Press. Croxall, J.P., 1993. Diet. In Antarctic seals (ed. R.M. Laws), pp. 268^293. Cambridge: Cambridge University Press. Desportes, G., 1985. La nutrition des odontoce'tes en Atlantique nord-est (co“ tes Franc aises ^ |“ les Feroe« ). PhD thesis, Universite¤ de Poitiers, Poitier, France. Gess, F.W., 1984. The smaller cetaceans of the southeast coast of southern Africa. In Annals of the Cape Provincial Museums, vol. 15, pp. 317^352. Grahamstown: Cape Provincial Museums. Goujon, M., 1996. Captures accidentelles au ¢let maillant de¤ rivant et dynamique des populations de dauphins au large du Golfe de Gascogne. PhD thesis, Ecole Nationale Supe¤rieure d’Agronomie de Rennes, Rennes, France. Ha«rko«nen, T.J., 1986. Guide to the otoliths of the bony ¢shes of the northeast Atlantic. Hellerup: Danbiu ApS. Jobling, M. & Breiby, A., 1986. The use and abuse of ¢sh otoliths in studies of feeding habits of marine piscivores. Sarsia, 71, 265^274. Miyazaki, N., Kusaka, T. & Nishiwaki, M., 1973. Food of Stenella coeruleoalba. Scienti¢c Report of the Whales Research Institute, 25, 265^275. Nesis, K.N., 1987. Cephalopods of the world: squids, cuttle¢shes, octopus, and allies (ed. B.S. Levitov). Neptune City, NJ: T.F.H. Publications, Moscou.
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Food and feeding ecology of the striped dolphin in north-east Atlantic
Olson, R.J. & Boggs, C.H., 1986. Apex predation by yellow¢n tuna (Thunnus albacares): independent estimates from gastric evacuation and stomach contents, bioenergetics, and cesium concentration. Canadian Journal of Fisheries and Aquatic Sciences, 43, 1760^1775. Pierce, G.J. & Boyle, P.R., 1991. A review of methods for diet analysis in piscivorous marine mammals. Oceanography and Marine Biology. Annual Review, 29, 409^486. Quinn, G.P. & Keough, M.J., 2002. Experimental design and data analysis for biologists. Cambridge: Cambridge University Press. Reynold, J.C. & Aebischer, N.J., 1991. Comparison and quanti¢cation of carnivore diet by faecal analysis: a critique, with recommendations, based on a study of the fox Vulpes vulpes. Mammal Review, 21, 97^122.
Journal of the Marine Biological Association of the United Kingdom (2006)
Roe, H.S.J., Angel, M.V., Badcock, P., Domanski, P.T., Pugh, P.R. & Thurston, M.H., 1984. The diel migration and distributions within a mesopelagic community in the North East Atlantic. Progress in Oceanography, 13, 244^511. Spitz, J., Richard, E., Meynier, L., Pusineri C. & Ridoux, V., in press. Dietary plasticity of the oceanic striped dolphin, Stenella coeruleaoalba, in the neritic Bay of Biscay. Journal of Sea Research. Wu«rtz, M. & Marrale, D., 1993. Food of striped dolphins, Stenella coeruleoalba, in the Ligurian Sea. Journal of the Marine Biological Association of the United Kingdom, 73, 571^578.
Submitted 5 September 2005. Accepted 16 January 2006.
Food and feeding ecology of the striped dolphin, Stenella coeruleoalba, in the oceanic waters of the north-east Atlantic Julien Ringelstein*, Claire Pusineri*, Sami HassaniO, Laureline Meynier*P, Re¤mi Nicolas* and Vincent Ridoux*P$ *Centre de Recherche sur les Ecosyste'mes Littoraux Anthropise¤s, UMR6217, Universite¤ de La Rochelle, 17071 La Rochelle cedex, France. OLaboratoire d0 Etude des Mammife'res Marins, Oce¤anopolis, BP411, 29275 Brest cedex, France. P Centre de Recherche sur les Mammife'res Marins, Universite¤ de La Rochelle, 17071 La Rochelle, France. $ Corresponding author, e-mail: [email protected]
The food and feeding ecology of the striped dolphin, Stenella coeruleoalba, in the oceanic waters of the north-east Atlantic were studied using the stomach contents of 60 striped dolphins caught in the albacore drift-net ¢shery throughout the summer months of 1992 and 1993 o¡ the Bay of Biscay. Thirty-eight per cent of these dolphins were calves (0^1 years old), 25% were juveniles (2^8) and 37% were mature adults (9^32, of which 7 females and 14 males). The diet was found to be primarily composed of ¢sh (39% by mass (M)) and cephalopods (56% M) and secondarily of crustaceans (5% M). The most signi¢cant ¢sh family identi¢ed was the lantern¢sh (24% M) with Notoscopelus kroeyeri and Lobianchia gemellarii being predominant. Among squid, the oceanic Teuthowenia megalops and Histioteuthis spp. were the most signi¢cant. The pelagic shrimp Sergastes arcticus and Pasiphaea multidentata were the most prevalent crustaceans. Prey sizes ranging from 30 to 170 mm accounted for 80% of the prey items while 80% of the reconstituted biomass consisted of prey measuring between 60 and 270 mm. Prey composition and size-range di¡ered slightly with sex and age or body size of the dolphins. The state of digestion of food remains suggested that predation took place at dusk or during the early hours of the night on which the dolphins were caught.
INTRODUCTION The striped dolphin (Stenella coeruleoalba, Meyen, 1833) is a small cetacean distributed worldwide in tropical and warm-temperate waters (Archer, 2002). In the North Atlantic, the species ranges to the west from Newfoundland to the Caribbean with eastern limits from Norway to the Gulf of Guinea (Archer & Perrin, 1999). The species has been reported at water temperatures of 10 to 268C, although most records show temperatures varying from 18 to 228C (Archer & Perrin, 1999). The habitat of the striped dolphin is mainly oceanic, with few incursions over the continental shelf being recorded throughout the range of the species (Archer, 2002). In the water column, the striped dolphin is purported to dive as deep as 200^700 m; however, investigation of its diving and foraging behaviour is not extensive (Archer, 2002). In the north-east Atlantic, the striped dolphin is part of a pelagic top predator community. This is composed mainly of two delphinids, the common Delphinus delphis and the striped dolphin S. coeruleoalba, the blue shark Prionace glauca, the albacore tuna Thunnus alalunga, the sword¢sh Xiphias gladius, and several smaller ¢sh predators including juvenile wreck¢sh Polyprion americanus and the Atlantic pomfret Brama brama. The status of each of these species with regards to ¢sheries is very di¡erent. The albacore tuna and the sword¢sh are target species of directed ¢sheries, the blue shark, the wreck¢sh and the Atlantic pomfret are secondary catches in the Journal of the Marine Biological Association of the United Kingdom (2006)
tuna ¢shery and are only partially marketed, whereas the two dolphins are protected species. The proper management of such a composite set of species requires understanding the ecology of each species and its relationships within the community, notably in terms of pelagic
Figure 1. Sampling location.
Journal of the Marine Biological Association of the United Kingdom (2006)
14 20
50.1^0.2
50.1^0.2
50.1^50.1
50.1^0.1 2.4^5
0.1
0.1
50.1
50.1 3.5 62.1
6.6
13.1
1.6
6.6 59.0 93.4
9 0
1
4
50.1^0.1
14.8 42.6 1.6 19.7 14.8
50.1
5.1 6.3 8.2 3.5 14.0 0.9 50.1 7.8 0.6 3.0
52.5 52.5 45.9 49.2 75.4 37.7 6.6 54.1 18.0 54.1
16 111
50.1^0.2 0.3^1.2
6.6
0.1 0.8
11.5 26.2
163
0.5^1.2
149
22 190 1 123 42
0.8
49.2
0.7^1.8
100 164
50.1^0.2 0.7^2.2 50.1^50.1 0.3^1.3 0.1^0.7
1.1
44.3
0.3^3.9 0.3^2.7
34
0.1 1.3 50.1 0.7 0.3
1.9 1.2
32.8 21.3
0.1^0.3
73
N
294 365 674 234 718 217 8 465 111 0
0.2
13.1
0.1^0.8
95% CI
1.6^10.4 1.7^13.4 4.2^12.5 0.7^7.9 6.9^21.8 0.5^1.4 50.1^0.1 2^17.8 0.2^1.2 2^4.6
0.4
13.1
%N
137.6 11.9
150.0
112.0 13.3
116.2 54.2
195.1 19
162.8 35.5 138.6 28.1 415.0 180.4 53.6 132.4 39.8
20.8 4.1 61.9 9.2 56.8 17.6 46.5 13.7 52.5 23.8 76.6 16.5 41.8 7.1 52.3 14.4 58.0 10.6
90.0 51.9 77.0 26.6
138.4 46.4
150.7 44.8
31.3 8.1 54.2 13.4
149.5 23.1
79.8 17.6
Mean SD
3.7 4
Mean SD
0.4 0.2 3.9 3.8
70.2^318.3 87.3^288.9
96.5^206.0 45.4^257.9
15.0^65.0 37.4^91.5 5.2^99.8 22.5^143.8 16.5^172.7 51.2^116.7 35.1^54.6 26.8^144.0 36.2^112 5.8 3.1 2.2 1.5 22.0 6.6 6.9 2.5 4.5
0.1 0.2 2.9 1.4 3.9 2.7 1.7 3.7 3.1 7.1 7.4 4.8 2.5 0.4 1.3 2 4.3 0.8 2.7
32.4^157.5 11.5 7.4 10.7^164.5 8.9 4.5
82.4^332.4 13.9 15.3
18.0^303.1 21.4 6.4
5.4^49.5 28.8^97.1
98.0^198.4 38.6 19.7
52.0^157.7
Range
13.6
9.5 1.1
116.9^151.8 45.1 3.9 3.7
97.2^135.0
26.3^206.5 13.0 8.0
38.3^49.8
8.3^11.5
4.5^27.8
6.1^54.8
0.3^35.9 0.5^24.6
0.2 2.4 38.9
50.1
0.2
0.2
0.2
0.1 0.5 0.3 0.8 0.1
0.1 3.2 5.7 1.1 8.2 0.8 50.1 1.9 0.5 1.5
50.1^2.7 0.4^9.8 50.1^17.2 0.1^55.5 0.1^75.8 2.4^27.5 2.1^3.3 0.1^28.2 1.1^6.5 1.2^10.0 0.1^15.9
0.2 1.7
1.9
3.5^20.4 2.1^29.6
0.6^106.4
4.3
0.1 0.8
50.1^1.1 0.4^20.6 2.6^43
1.5
0.2
%M reconstituted
0.1^0.5 1.2^3.8
50.1^50.1
0.1^0.3
50.1^0.4
50.1^0.4
50.1^0.2 0.2^0.8 50.1^0.9 0.3^1.7 50.1^0.3
50.1^0.2 0.7^7.5 2.5^9 0.5^2 4.1^13 0.4^1.5 50.1^50.1 1^3.2 0.2^0.9 0.9^2.5
0.1^0.5 0.2^3.7
1^2.9
2.3^7
50.1^0.3 0.2^1.4
0.5^2.3
50.1^0.3
95% CI
Composition by mass
7.3^98.4
0.8^31.0
Range
Mass (g)
176.5^221.7 23.6 22.1
Length (mm)
6.6 14.8 95.1
13.1
1.6
14.8 42.6 1.6 19.7 14.8
39.3 49.2 44.3 31.1 72.1 36.1 4.9 44.3 18 47.5
9.8 23.0
49.2
6.6
8.2 16.4
11.5
13.1
% Occurrence
0.1 0.7 71.8
0.2
50.1
0.2 2.3 50.1 1.3 0.6
5.1 6.7 14 1.7 20.2 1.4 50.1 7.1 1.1 3.1
0.1 0.8
1.4
0.5
1.3 1.3
0.2
0.6
%N
(Continued)
0.4 0.5 54.6
0.3
50.1
0.2 0.9 0.5 0.9 0.3
0.1 3.4 10.1 1 13.3 1.9 50.1 2 6.5 1.5
0.4 1.8
3.5
2.4
0.1 0.8
1.5
0.5
%M reconstituted
Fresh fraction (N¼8700; M¼47449.8)
J. Ringelstein et al.
Alepocephalidae Xenodermichthys copei Platytroctidae Unid. Platytroctidae Sternoptychidae Maurolicus muelleri Argyropelecus olfersi Chauliodontidae Chauliodus sloani Stomiidae Stomias boa ferox Bathylagidae Bathylagus greyae Unid. Bathylagidae Myctophidae Benthosema glaciale Ceratoscopelus maderensis Lobianchia gemellarii Myctophum puntatum Notoscopelus kroeyeri Symbolophorus veranyi Diaphus metoclampus Lampanyctus spp. Electrona risso Unid. Myctophidae Paralepididae Macroparalepis a⁄nis Arctozenus risso Paralepis atlantica Paralepis coregonoides Unid. Paralepididae Serrivomeridae Serrivomer beani Scomberesocidae Scomberesox saurus Chiasmodontidae Unid. Chiasmodontidae Gempylidae Nesiarchus nasutus Nomeidae Cubiceps gracilis Unidenti¢ed ¢sh Total ¢sh
% Occurrence
Composition by number
Total composition (N¼15129; M¼82124.7)
Table 1. Diet composition of the striped dolphin in the oceanic Bay of Biscay. % N is the percentage by number of the prey, % M the percentage reconstituted biomass. Lengths are standard length for ¢sh, dorsal mantle length for cephalopods and total length without rostrum for crustaceans.
910 Food and feeding ecology of the striped dolphin in north-east Atlantic
Journal of the Marine Biological Association of the United Kingdom (2006)
Unid., unidenti¢ed.
Acanthephyra purpurea Systellapsis debilis Acanthephyra spp. Unidenti¢ed crustaceans Total crustaceans
Acanthephyra pelagica
Pasiphaea silvado Pasiphaea spp. Oplophoridae
Pasiphaea multidentata
Hyperiidae Unid. Hyperiidae Euphausiidae Meganyctyphanes norvegica Unid. Euphausiidae Peneaeidae Funchalia woodwardii Sergestidae Sergestes arcticus Sergia robusta Pasiphaeidae
Octopoteutidae Octopoteuthis sp. Onychoteuthidae Onychoteuthis banksi Ancistroteuthis lichtensteini Gonatidae Gonatus steenstrupi Pholidoteuthidae Pholidoteuthis sp. Histioteuthidae Histioteuthis bonellii Histioteuthis reversa Histioteuthis corona Brachioteuthidae Brachioteuthis riisei Ommastrephidae Unid. Ommastrephidae Chiroteuthidae Chiroteuthis imperator Chiroteuthis sp. Cranchiidae Teuthowenia megalops Sepiolidae Heteroteuthis dispar Unid. Sepiolidae Unidenti¢ed cephalopods Total cephalopods
1.4 50.1 50.1
0.1 0.5 0.1 50.1 0.1 5.3
34.4 1.6 1.6
6.6 14.8 6.6 1.6 6.6 70.5
0.1 0.2 50.1 32.4
8.2 13.1 1.6 96.7
1.7 0.5
10.9
83.6
29.5 23.0
50.1 50.1
6.6 1.6
0.2
50.1
6.6
18.0
50.1^0.1 50.1^50.1
9.9
77.0
0.1 50.1
50.1^0.1
50.1 5.2 1.1
1.6 80.3 36.1
9.8 6.6
50.1^50.1 3.9^7 0.5^2.1
50.1
1.6
0.6
50.1^50.1
3.7
83.6
19.7
50.1^0.1 0.7^1.6
50.1 1.1
6.6 49.2
50.1^0.3 0.2^1 50.1^0.2 50.1^0.1 50.1^0.1
0.7^2.4 50.1^50.1 50.1^0.1
0.5^3.1 0.2^0.9
5 47 12 3 0
123 1 1
128 58
19
10 4
50.1^0.3 50.1^0.1 0.1^0.3
22
10 30
50.1^0.1 50.1^0.2 50.1^50.1
0.2^1.1
1099
5 1
4
869
1 624 115
1
486
5 163
13
8.6^13.7
7^13.5
2.6^5.2
50.1^0.2
0.1
18.0
63.4 2.7 63.8 10.3 43.3 5.7 55.4 4.7
97.9 25.5 114.6 91.9
49.2 5.8 71.7 5.7
109.4 15.1
27.7 3.8 24.2 3.7
16.0 4.3
15.8 0.1 15.9 0.3
106.5 25.5
99.2 9.8 40.7
102.8 68.6
25.7 22.5
265.7 25.7 8.5 23.5 8
124.4
105.6 34
71.3 53.4 57.1 15.8
27.6 49.6
1.9 1.9
501.6 35.4 11.7 42.3 13.9
0.2 0.1 0.1 50.1
0.1 0.1
1.5 0.1 1.6 0.2 19.7
59.1^66.0 5.6^85.2 31.9^51.4 51.2^61.9
6.9^151.8
33.6^72.5 45.2^86.3
2.1 0.3 2.3 1 0.9 0.3 1.4 0.3 6.0
7.3 1.9 11.2 5.7
4.0 4.5 1.6 0.7
94.2^142.5 17.8 9.5
19.8^33.1 18.7^28.1
11.0^23.7
15.7^15.9 15.5^16.6
41.2^200.2 16.4 10.7
81.4^108.5 25.4 6.8 6.7
64.9^243.8 152.3 101.7
15.0^78.0
7.8^56.9 11.6^61.1
144.8
15.8^282.4 43.9 35.6
4.0^128.5 26.1 23.2 31.0^122.7 27.5 44.6
6.4^198.6 81.9 84.9
1.7^2.3 0.1^6.0 0.5^1.4 1.1^1.9
1.9^14.6
3.2^25.3 0.8^3.5
8.2^38.6
0.1^0.3 0.1^0.2
50.1^0.4
1.4^1.6 1.3^2.0
0.9^73.9
13.4^32.5
96.3^361.5
1.1^8.3
10.8^78.9 20.3^106.8
5.0^445.3
0.2^59.5 0.8^326.0
15.4^331.6
50.1 0.2 50.1 50.1 0.1 5.2
1.8 50.1 50.1
2.3 0.2
0.6
50.1 50.1
50.1
50.1 50.1 50.1 55.9
31.9
0.1 50.1
1.1
0.2
0.2 4.6 8.5
0.2
2.4
0.2 5.5
0.9
50.1^0.1 0.1^0.4 50.1^50.1 50.1^50.1 50.1^0.1
0.7^3.2 50.1^50.1 50.1^0.1
0.8^4.6 0.1^0.3
0.3^1.1
50.1^50.1 50.1^50.1
50.1^50.1
50.1^50.1 50.1^50.1 50.1^0.1
25.9^38.5
50.1^0.3 50.1^0.1
0.3^2.3
0.1^0.3
50.1^0.6 3.6^6.1 3.9^14.6
50.1^0.6
1.7^3.4
50.1^0.4 3.2^8.5
0.4^1.8
6.6 14.8 6.6 50.1 0 59
1.6
21.3
24.6 11.5
9.8
9.8 6.6
19.7
8.2 13.1 3.3 96.7
45.9
1.6
1.6
73.8
1.6 70.5 27.9
18.0
6.6 11.5
6.6
50.1 0.8 0.1 50.1 0 6.1
0.1
1.2
1.9 0.4
0.1
0.2 0.1
1
0.1 0.2 0.1 22.1
1.3
50.1
50.1
13.2
50.1 5.9 0.8
0.4
50.1 0.2
0.1
50.1 0.4 50.1 50.1 0 5.4
0.1
1.7
2.6 0.2
0.5
50.1 50.1
50.1
50.1 0.1 0.1 40
4.1
50.1
0.8
8.4
0.4 14.3 6.1
3.5
0.1 1.8
0.5
Food and feeding ecology of the striped dolphin in north-east Atlantic J. Ringelstein et al. 911
912
J. Ringelstein et al.
Food and feeding ecology of the striped dolphin in north-east Atlantic
Figure 2. Prey length-distribution of all species combined. Lengths are standard length for ¢sh, total length for cephalopods and total length without rostrum for crustaceans.
habitat, of resource utilization and partitioning and of its role in the upper food web. In all cases, the quanti¢cation of the diet is paramount to the understanding of these processes. The feeding ecology of the striped dolphin has mainly been investigated in Japan, South Africa, the Mediterranean Sea and the Bay of Biscay (Miyazaki et al., 1973; Desportes, 1985; Wu«rtz & Marale, 1993; Spitz et al., in press). Cephalopods and ¢sh constitute the bulk of the diet and the typical prey pro¢le of the striped dolphin is a pelagic, gregarious, vertically migrating, small sized organism. Data on the food of the striped dolphin in the North Atlantic are limited to stranded individuals and therefore re£ect the species feeding habits in neritic and coastal waters (Desportes, 1985; Spitz et al., in press). Although in many regions stranded cetaceans incorporate a large proportion of by-caught individuals, they are often considered to be biased towards ill or debilitated individuals. In contrast, the present study is based only on bycaught animals which are presumably healthy. Thus, the aim of this work is to provide a quantitative analysis of the diet of the striped dolphin in the oceanic waters of the
north-east Atlantic (longitude 408050 N to 508290 N and latitude 128190 W to 218190 W) and to describe its variability, based on animals caught in the species’ characteristic o¡shore habitat.
MATERIALS AND METHODS Sampling
This work is based on analysis of the stomach contents of 60 striped dolphins caught in an albacore drift-net ¢shery during the summer months (early June to late September) of 1992 and 1993, as part of a study on the impact of this ¢shery on small cetaceans (Goujon, 1996). The study area was located o¡ the Bay of Biscay between longitude 408050 N and 508290 N and latitude 128190 W to 218190 W (Figure 1). The dolphins in question were by-caught at night in commercial drift-nets 2.5 km long with a 20 m vertical spread. They ranged in age from 0+ to 32 y-old and in size from 112 to 226 cm, corresponding to three predominant age-categories: 38% of the individuals were calves (0^2 y-old), 25% were juveniles (2^8), and 37%
Figure 3. Main prey length-distribution. Lengths are standard length for ¢sh and dorsal mantle length for cephalopods. Journal of the Marine Biological Association of the United Kingdom (2006)
Food and feeding ecology of the striped dolphin in north-east Atlantic J. Ringelstein et al. 913 were mature adults (8^32). Among adults, 34% were females and 67% males (Goujon, 1996). The stomachs were dissected onboard and stored frozen at 7208C in polythene bags awaiting further analysis. Sample analysis
Sample analysis was aimed at describing the diet in terms of prey occurrence, relative abundance, reconstituted mass and size-distribution. It was carried out according to a general procedure which is now standard for marine top predators (Pierce & Boyle, 1991; Croxall, 1993). Details are provided in similar works carried out previously in the same area (Spitz et al., in press). Brie£y, the stomach contents were washed through a sieve of 0.2-mm mesh size, the diagnostic parts and fresh prey recovered and identi¢ed to the lowest taxonomic level using published guides (Clarke, 1986; Ha«rko«nen, 1986) and our own reference collection. To minimize overestimation of prey resistant to digestion (e.g. cephalopod beaks: Bigg & Fawcett, 1985), each prey item was scored on a scale speci¢c to the main prey type (¢sh, cephalopods, crustaceans), according to their state of decomposition. This allowed us to determine a ‘fresh fraction’ that would provide a better representation of the composition of the ingested prey than the total stomach content. Diagnostic hard parts such as beaks, otoliths, and carapaces were measured with a digital Vernier calliper ( 0.02 mm), according to accepted standards (Clarke, 1986; Ha«rko«nen, 1986). A random sub-sample of up to 30 diagnostic hard parts per prey species per stomach sample was measured. Individual prey body length and mass were then calculated using relationships either from the literature (Clarke, 1986; Ha«rko«nen, 1986), or ¢t to measurements performed on specimens in our reference collection. For cephalopods, the standard dorsal mantle length (DML) was used in the general description of the diet (Table 1); however, a total body length including arm length was derived from total length to mantle length ratios obtained from published illustrations of the corresponding species (Nesis, 1987) and used in the ¢gure representing overall prey size-distributions as it quali¢es the prey size targeted by the dolphin (Figure 2) better than DML. The occurrence of a given prey taxon was the number of stomachs in which the taxon was observed and its relative abundance was the number of items of the same taxon found in the sample set. The reconstituted biomass of a taxon was the product of the number of individuals in each stomach and its average reconstituted body mass, summed throughout the sample set. Each of these indices was calculated separately for the total content and the fresh fractions. Standard deviations for the compositions by number (% N) and by mass (% M) were generated by bootstrapping (Reynolds & Aebischer, 1991). The bootstrapping routine was written using the R software. Random samples were drawn with replacement, and the procedure was repeated 300 times. An explanatory diagram, the modi¢ed Costello diagram (Amundsen et al., 1996), was built for each predator. This tool is used to characterize diet variability of a predator graphically by plotting prey speci¢c importance for each prey taxa (% Pi, Equation 1) against Journal of the Marine Biological Association of the United Kingdom (2006)
Figure 4. Costello diagram, a scatterplot of all prey species according to their occurrence and their importance by mass.
frequency of occurrence (% Occ, Equation 2) on a twodimensional graph (Figure 4). In the upper left corner of the diagram, each prey species occurs rarely but accounts for a large proportion of the diet when present; hence, if most prey species concentrate here, the predator is characterized by high between-individual variability. In the upper right corner of the diagram, a single prey is present in all individuals and accounts for the total diet. In this case, all predator individuals rely on the same resource. In the lower right corner, prey species occur at high frequency but each only accounts for a small proportion of the food when present. This suggests high within-individual variability in prey preference and low between-individual variability since all individual predators prey upon the same species assemblage. Finally, in the lower left corner of the diagram, individual prey species display both a low occurrence and low relative importance when present. If most prey species concentrate here, the predator shows both within and betweenindividual variability: % Pi ¼ (i Mi /Sti Mti ) 100
(1)
% Occ ¼ (ni /N) 100
(2)
where Mi is the contribution (by mass in this study) of prey taxa i (at species level, in this study) to stomach content, Mti is the total stomach content weight in only those predators with prey i in their stomach; ni is the number of stomachs in which prey taxon i was found and N the total number of stomachs. Discriminant function analyses (DFAs) were performed to look at intra-speci¢c variability of diet composition between gender ^ maturity categories. Discriminant function analysis generates a set of linear combinations (called the discriminant functions) of explanatory variables (here the prey families) that maximizes the discrimination between pre-de¢ned groups (here the gender ^ maturity categories) (Quinn & Keough, 2002). The data used here were the diet composition by mass at prey family level of all individual samples. The maturity
914
J. Ringelstein et al.
Food and feeding ecology of the striped dolphin in north-east Atlantic
Figure 5. Prey/predator length correlation.
categories were determined from the age of the individuals: calves 52 y-old, juveniles 5257 y-old; and adults 57. Age was determined by reading growth layer groups on teeth slides (Goujon, 1996).
RESULTS General description
About 21% of the available stomachs were full and 79% were half full or less. The total mass of examined food material was 17,250 g which represented an average stomach content of 314 g (N¼60; range 1^2,688). Most food material found was highly digested and the total reconstituted mass was 82,125 g, i.e. 4.8 times the mass of food material actually recovered in the stomachs. Diet composition
The diet of the striped dolphin consisted mainly of ¢sh and cephalopods, but also included crustaceans (occurrence: 93.4%, 96.7% and 70.5% respectively). A total of
9410 ¢sh remains was found, belonging to 55 species of 13 families and corresponding to a reconstituted mass of 31,946 g. The remains of 4917 cephalopod individuals were identi¢ed, corresponding to 13 species of 9 families and 45,908 g of reconstituted mass, in addition to 802 crustaceans of 13 species and 6 families, amounting to a reconstructed mass of 4270 g. Hence, the total diet was constituted of 62.1% ¢sh remains by number and 38.9% by mass, but these ¢gures were increased to 71.8% by number and 54.6% by reconstituted mass in the fresh fraction alone. Myctophid were by far the most signi¢cant ¢sh family, representing 49.4% N of all prey items and 23.0% M of the total diet (and as much as 64.8% N and 42.6% M in the fresh fraction). At least nine di¡erent species were found, with Notoscopelus kroeyeri and Lobianchia gemellari being the most important (Table 1). The cephalopods accounted for 32.4% by number and 55.9% by mass of the total diet, but only 22.1% by number and 40.0% by mass of the fresh fraction. They were represented by at least 15 species, of whichTeuthowenia megalops, Brachioteuthi riissei, Histioteuthis reversa and Gonatus steenstrupi were the most signi¢cant. In the total diet, T. megalops ranked ¢rst by mass among all cephalopods, whereas H. reversa and B. riisei ranked ¢rst and second respectively in the fresh fraction (Table 1). Crustaceans made up 5.3% by number and 5.2% by mass of the total diet, and 6.1% by number and 5.4% by mass of the fresh fraction. The sergestid Sergestes arcticus was the most prevalent species followed by the pasiphaeid Pasiphaea multidentata (Table 1). Length-distributions
The striped dolphins under study fed on prey ranging in size from 10 to 540 mm. Within this extended prey sizerange, the distributions by relative abundance and by relative mass showed quite di¡erent pro¢les (Figure 2). Eighty per cent of the prey items measured between 30 and 170 mm with a major mode from 30^100 mm and a very £at secondary mode at 100^200 mm, whereas 80% of the reconstituted mass was accounted for by size-classes from
Figure 6. Intraspeci¢c diet variability through factorial discriminant analysis of gender^maturity groups (&, adult males; &, adult females; *, juveniles; *, calves).
Journal of the Marine Biological Association of the United Kingdom (2006)
Journal of the Marine Biological Association of the United Kingdom (2006)
Brachioteuthidae Sepiolidae Sepiidae Chiroteuthidae Cranchidae Gonatidae Hitioteuthidae Loliginidae Lycoteuthidae Ommastrephidae Onychoteuthidae Other cephalopods Total cephalopods Total crustaceans
Atherinidae Bathylagidae Belonidae Carangidae Chauliodontidae Clupeidae Emmelichthydae Engraulidea Gadidae Gonostomatidae Merluccidae Mugilidae Myctophidae Nemichthydae Paralepididae Sparidae Sternoptychidae Stomiatidae Alepocephalidae Gobiidae Other ¢sh Total ¢sh
%Nb
%Nb
0.9 6.7 9.9 0.4 0.3 0.9 19.3 50.1
0.1 0.1
2.3 80.4
34.3 35.2 37.5
0.9
1.6 27.5
3.4 1.4 0.8 7.28 1.6
1.3 0.4
0.8 91.0
27.4 6.3 0.5 49.8 1
15.3 0.3
49.2
14.2 1.3 3.8
2.9 23.8 11.9
0.4
1.7
15.6
17.6 3.6 0.7
66.3
3.9
1.3
1.3 19.0
1.1
3.1
%M
50.1
2.8 31.2
0.4
0.3
%Nb
Wu«rtz & Marrale, 1993 Mediterranean Sea N¼23 strandings
2.7 9.1
2.2
2.1
Miyazaki et al., 1973 Japan N¼27 incidental catches
Gess, 1984 South Africa N¼15 strandings and incidental catches
6.8 8 50.1
1.6
0.2 0.1 0.4 0.3 2.8
1.0
11.5 92.0
1.0 5.7
66.9
2.1
2.9
8.6
%Nb
28 50.1
7.7
2.3 0.6 5.1 0.3 11.7
0.3
8.4 72.0
1.4 5.1
49.8
6.6
2.9
4.3
%M
Desportes, 1985 French Atlantic coasts N¼34 strandings and incidental catches
Table 2. Diet composition found in the literature. % N is the percentage by number of the prey, % M the percentage reconstituted biomass.
0.8 8.7 0.5
0.6
0.1 1.4 0.1 1.3
50.1 39 50.1
16.2
0.3 17.5 0.2 4.1
0.1 0.5 0.1
50.1 0.7 50.1 61.0 0.1 24.3 1.1 91.2 0.2 3.9 0.3
0.3 50.1
1.7 1.8 0.4
0.2 43.6
12.3
%M
0.5 0.5
0.5 0.1 2.1
0.2 45.2
16.6
%Nb
Spitz et al., in press French Atlantic coast N¼32 strandings
Food and feeding ecology of the striped dolphin in north-east Atlantic J. Ringelstein et al. 915
916
J. Ringelstein et al.
Food and feeding ecology of the striped dolphin in north-east Atlantic
60 to 270 mm, with two modes at about 40^110 mm and 150^250 mm. This latter mode resulted from the larger size-classes, which, although they only made up the tail end of the relative abundance distribution, represented a signi¢cant part of the reconstituted mass. Among the main prey species (Figure 3), the most numerous lantern¢sh N. kroeyeri and L. gemellari contributed to the ¢rst mode of the overall distribution whereas the cephalopod T. megalops, together with other rarer large species of ¢sh and squid, contributed to the second mode. All crustaceans contributed to the ¢rst mode. Costello diagram
Plotting speci¢c importance against occurrence for all prey species (Figure 4) shows that there is not a single pivotal species; instead, an assemblage of mesopelagic ¢sh and squid is targeted by most individual dolphins. Group 1 (G1) is made up of all the species characterized by both a low occurrence and a low speci¢c importance by mass. Group 2 (G2) constitutes the assemblage of common prey species that display intermediate occurrence (25%5Occ560%); it is made up of a combination of mesopelagic species. Finally, Group 3 (G3) is composed of the most recurrent (60%5Occ580%) prey species which included one myctophid and four oceanic squids. Diet variability
Intra-speci¢c diet variability examined across body size-range and between gender ^ maturity categories (calves, juveniles, adult males and adult females) showed weak yet signi¢cant di¡erences. In spite of extensive variations between individuals, the prey size-range increased with dolphin body length (average prey length¼0.03+2.09dolphin length; R2 ¼0.09; P¼0.025; Figure 5). Similarly, diet composition also changed slightly as shown by the DFA performed on stomach composition by mass. The four gender ^ maturity categories segregated fairly well, with the juveniles in the middle of the projection, suggesting that their diet was intermediate between the calf diet and the male and female adult diets (Figure 6, left side). The length of the discriminant function vectors (Figure 6, right side) was generally shorter than 0.5 suggesting that dietary segregation between gender or maturity categories was far from complete. However, it appeared that two crustacean families (Sergestidae and Oplophoridae) together with the gelatinous squid family Cranchiidae are principally part of the calf diet, whereas the longest vectors associated several non-myctophid ¢sh families to the adult female diet. Finally, very few and only short vectors, including the myctophids, headed towards the male part of the scatterplot suggesting that males simply focus their foraging more heavily on this family than the other categories do.
DISCUSSION General assessment of the study
The present work was the ¢rst quantitative analysis of the diet of the striped dolphin in oceanic habitats of the north-east Atlantic. The diet was found to be primarily composed of ¢sh and cephalopods, and secondarily of Journal of the Marine Biological Association of the United Kingdom (2006)
crustaceans. The lantern¢sh was the most important ¢sh family with predominance of Notoscopelus kroeyeri and Lobianchia gemellarii. Among squid, the oceanic Teuthowenia megalops and Histioteuthis spp. were the most signi¢cant. The pelagic shrimps Sergestes arcticus and Pasiphaea multidentata were the most prevalent crustaceans. Prey individuals measuring 30 to 170 mm accounted for 80% of the prey items and sizes from 60 to 70 mm represented 80% of the reconstituted biomass. Prey composition and size-range di¡ered slightly with sex and age or body size of the dolphins. In general, the food remains were in a state of advanced digestion suggesting that predation took place in the early part of the night on which the dolphins were caught. These results were limited by several constraints. In particular, sampling was determined by the spatiotemporal characteristics of the ¢shery within the study area. More individuals were collected from the north-east sector of the area, close to the continental slope, than elsewhere (Figure 1). For the same reason, samples were only collected at the end of the night, from May to September. The analytical procedure was standard and all the limitations associated with stomach content analyses, notably the biases due to di¡erential transit time in the stomach extensively discussed elsewhere (e.g. Bigg & Fawcett, 1985; Jobling & Breiby, 1986), are fully acknowledged here. However, we believe that scoring the state of digestion of the remains of each prey and considering the fresh fraction alone, as proposed here, partly circumvents this di⁄culty. Finally, the sample size of 60 individuals proved to be su⁄cient to describe the diet of the striped dolphin at an acceptable level of certainty as shown by the 95% con¢dence intervals that are provided in Table 1. Comparison with previous research
The food of the striped dolphin has mainly been investigated in Japan, South Africa, the Mediterranean Sea and the neritic part of the Bay of Biscay (quantitative studies: Miyazaki et al., 1973; Desportes, 1985; Wu«rtz & Marale, 1993; Spitz et al., in press). Cephalopods and ¢sh constitute the bulk of the diet at all locations (Table 2), even if crustaceans and annelids were also found. The dominant prey pro¢le arising from these studies is an epi- or mesopelagic, comparatively small-sized, schooling organism. The gut content of animals collected at sea in oceanic habitats (Miyasaki et al., 1973; this study) were entirely composed of oceanic prey taxa, whereas animals found stranded (Desportes, 1985; Spitz et al., in press) show a mixture of oceanic and shelf prey taxa, with the latter often predominating. This suggests that the population segments that were sampled in oceanic habitats do not usually forage over the shelf, even when they are from areas located close to the shelf break, as was the case in the present study. In contrast, materials obtained from stranded dolphins suggest that these animals had been e⁄ciently foraging in both oceanic and shelf habitats. It is unclear if this represents a particular foraging strategy corresponding to a relatively ‘inshore’ sub-unit of striped dolphin populations, or if it is a minor component of a more widely shared foraging repertoire which would be overlooked by at-sea sampling and, on the contrary, overrepresented in stranding data. Lastly, one could consider
Food and feeding ecology of the striped dolphin in north-east Atlantic J. Ringelstein et al. 917 that material obtained from stranded dolphins might be biased because the source of samples would include more sick animals than materials obtained from ¢sheries. Striped dolphin prey size-ranges mostly overlapped in approximately the 3^30 cm range at all localities where this has been documented in detail (Miyasaki et al., 1973; Spitz et al., in press; present work), suggesting that the preferred prey pro¢le remains the same and, hence, that real plasticity in foraging strategy would be limited. However, it is perhaps noteworthy that, at the only neritic locality where this information has been documented, prey smaller than 10 cm provided less than 15% M of the food against *35% M in the present work. Intraspeci¢c variability
Little is known of intraspeci¢c variability in feeding habits. In the north-west Paci¢c, it was shown that immature striped dolphins concentrate on cepahalopods and take a wider diversity of ¢sh whereas adults preferentially eat ¢sh and crustaceans (Miyasaki et al., 1973). In the present work, it appears that the prey composition and size-distribution change slightly with age and gender. This may result from the ontogeny of diving capacity in calves and immatures and from nursing females being limited in their performance by their accompanying calf. Foraging strategy
The striped dolphin foraging depth-range is supposed to be in the 200^700 m strata, but little is known of its actual diving performances, either maximum or routine (Archer, 2002). In this context, all the species found in the present study live within this broad depth-range, and most of them are members of the vertically migrating mesopelagic fauna. Air breathing top predators can exploit this species assemblage either by foraging deeply during daylight, when these organisms are mostly inactive at depths forming the deep scattering layer, or by foraging at night in the surface layer where these organisms migrate nocturnally for their own feeding (Roe et al., 1984). In the absence of any telemetry data documenting a possible nycthemeral pattern in foraging activity, the prey item digestion conditions can shed some light on this issue. Here, most prey remains were highly digested and the stomach content did not contain much fresh material. From digestion time of small prey organisms observed in various predators (Bigg & Fawcett, 1985; Olson & Boggs, 1986), it appears that the dominant digestion condition observed in our samples is reached about 6 h after ingestion; since the samples were all collected during and at the end of the night, this suggests that most of the foraging activity took place at dusk or early night, when deep sea organisms move up to the surface layer. Interestingly, prey items in fresh condition were rare suggesting that the middle of the night might not be as favourable for foraging as dusk and early night are. This may result from prey organisms being less aggregated when they forage than when they migrate up to the surface layer. Niche breadth expressed as species diversity alone would be extremely wide in the present case, but expressed as the diversity of prey pro¢les could be much narrower, since most prey species are ecologically fairly similar. In Journal of the Marine Biological Association of the United Kingdom (2006)
the Costello diagram, the group of anecdotal species (lower left corner) encompasses all the rare species found in the analysis. At intermediate or higher frequency of occurrence, a more limited number of prey species constitutes the core of the diet. Most of these species occur in 40% to 80% of the samples suggesting that all individual striped dolphins forage on the same species assemblage. Hence, the niche breadth would be mainly accounted for by the speci¢c diversity of the mesopelagic fauna rather than by inter-individual variability in striped dolphin feeding strategy.
This work formed part of a large research programme on the role of pelagic top predators in the Bay of Biscay and adjacent Atlantic Ocean. Fundings from Ifremer and CNRS were obtained through the research project ‘Chantier Golfe de Gascogne, Programme National d0 Environnement Co“tier’. The identi¢cation of prey reference specimens was checked by JeanPaul Lagarde're (CREMA, l’Houmeau, France), Jean-Claude Que¤ro (Muse¤um d’Histoire Naturelle, La Rochelle, France), Yves Cherel (CNRS, Chize¤, France), and Begon‹a Santos Vasquez (University of Aberdeen, Aberdeen, UK). We are grateful to Gre¤goire Certain for computing the bootstrap program. All o¡ered their support, their knowledge and their time, and are gratefully acknowledged for their contribution.
REFERENCES Amundsen, P.A., Gabler, H.M. & Staldvik, F.J., 1996. A new approach to graphical analysis of feeding strategy from stomach contents data-modi¢cation of the Costello (1990) method. Journal of Fish Biology, 48, 607^614. Archer, F.I., 2002. Striped dolphin. In Encyclopedia of marine mammals (ed. W.F. Perrin et al.), pp. 1201^1203. New York: Academic Press. Archer, F.I. & Perrin, W.F., 1999. Stenella coeruleoalba. Mammal Spec, 603, 1^9. Bigg, M.A. & Fawcett, I., 1985. Two biases in diet determination of northern fur seals. In Marine mammals and ¢sheries (ed. J.R. Beddington et al.), pp. 277^282. Boston: George Allen and Unwin. Clarke, M.R., 1986. A handbook for the identi¢cation of cephalopod beaks. Oxford: Clarendon Press. Croxall, J.P., 1993. Diet. In Antarctic seals (ed. R.M. Laws), pp. 268^293. Cambridge: Cambridge University Press. Desportes, G., 1985. La nutrition des odontoce'tes en Atlantique nord-est (co“ tes Franc aises ^ |“ les Feroe« ). PhD thesis, Universite¤ de Poitiers, Poitier, France. Gess, F.W., 1984. The smaller cetaceans of the southeast coast of southern Africa. In Annals of the Cape Provincial Museums, vol. 15, pp. 317^352. Grahamstown: Cape Provincial Museums. Goujon, M., 1996. Captures accidentelles au ¢let maillant de¤ rivant et dynamique des populations de dauphins au large du Golfe de Gascogne. PhD thesis, Ecole Nationale Supe¤rieure d’Agronomie de Rennes, Rennes, France. Ha«rko«nen, T.J., 1986. Guide to the otoliths of the bony ¢shes of the northeast Atlantic. Hellerup: Danbiu ApS. Jobling, M. & Breiby, A., 1986. The use and abuse of ¢sh otoliths in studies of feeding habits of marine piscivores. Sarsia, 71, 265^274. Miyazaki, N., Kusaka, T. & Nishiwaki, M., 1973. Food of Stenella coeruleoalba. Scienti¢c Report of the Whales Research Institute, 25, 265^275. Nesis, K.N., 1987. Cephalopods of the world: squids, cuttle¢shes, octopus, and allies (ed. B.S. Levitov). Neptune City, NJ: T.F.H. Publications, Moscou.
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Food and feeding ecology of the striped dolphin in north-east Atlantic
Olson, R.J. & Boggs, C.H., 1986. Apex predation by yellow¢n tuna (Thunnus albacares): independent estimates from gastric evacuation and stomach contents, bioenergetics, and cesium concentration. Canadian Journal of Fisheries and Aquatic Sciences, 43, 1760^1775. Pierce, G.J. & Boyle, P.R., 1991. A review of methods for diet analysis in piscivorous marine mammals. Oceanography and Marine Biology. Annual Review, 29, 409^486. Quinn, G.P. & Keough, M.J., 2002. Experimental design and data analysis for biologists. Cambridge: Cambridge University Press. Reynold, J.C. & Aebischer, N.J., 1991. Comparison and quanti¢cation of carnivore diet by faecal analysis: a critique, with recommendations, based on a study of the fox Vulpes vulpes. Mammal Review, 21, 97^122.
Journal of the Marine Biological Association of the United Kingdom (2006)
Roe, H.S.J., Angel, M.V., Badcock, P., Domanski, P.T., Pugh, P.R. & Thurston, M.H., 1984. The diel migration and distributions within a mesopelagic community in the North East Atlantic. Progress in Oceanography, 13, 244^511. Spitz, J., Richard, E., Meynier, L., Pusineri C. & Ridoux, V., in press. Dietary plasticity of the oceanic striped dolphin, Stenella coeruleaoalba, in the neritic Bay of Biscay. Journal of Sea Research. Wu«rtz, M. & Marrale, D., 1993. Food of striped dolphins, Stenella coeruleoalba, in the Ligurian Sea. Journal of the Marine Biological Association of the United Kingdom, 73, 571^578.
Submitted 5 September 2005. Accepted 16 January 2006.
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